Abstract
One of the earliest stages in the process of pollination and fertilization in flowering plants is the recognition and acceptance or rejection of pollen grains alighting on the stigma of the recipient plant. Thus, these events involve some sort of interaction between male and female cells. Self-incompatibility (SI) is a mechanism employed by many plants whereby self-fertilization is prevented. This is under tight genetic control, usually a single gene, which is denoted the S-gene. These highly specific recognition/rejection events are both developmentally expressed and tissue specific. Studies aimed at the characterization of the S-gene, its product(s) and elucidation of the mechanism of how this system functions has therefore attracted some attention, especially since the advent of molecular biology. Much work has been carried out in an attempt to identify the molecules involved in SI, especially those on the female side. S-linked glycoproteins from styles and stigmas, and the genes that encode them, have been identified and cloned (Nasrallah et al. 1985; Anderson et al. 1986; McClure et al. 1989; berger et al. 1991). Less progress has been made with the pollen component. We initiated our study of the molecular and cellular basis of SI in Popover rhoeas L. (the Field Poppy) in 1985, with the aim of elucidating the mechanism of the SI response. Progress towards an understanding of the molecular basis of SI in this species has recently been made in several directions, and will be reviewed in this article.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
Similar content being viewed by others
References
Anderson, M.A., Cornish, E.C., Mau, S.-L., Williams, E.G., Hoggart, R., Atkinson, A. et al. (1986) Cloning of a cDNA for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata. Nature 321: 38–44.
Berridge, M.J. and Irvine, R.F. (1984) Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312: 315–321.
Campbell, J.M. and Lawrence, M.J. (1981a) The population genetics of the self-incompatibility polymorphism in Papaver rhoeas I. The number and distribution of S-alleles in families from three localities. Heredity 46: 69–79.
Campbell, J.M. and Lawrence, M.J. (1981b) The population genetics of the self-incompatibility polymorphism in Papaver rhoeas II. The number and frequency of S-alleles a natural population. Heredity 46: 81–90.
Cresti, M., Milanesi, C., Salvatici, P. and van Aelst, A.C. (1990) Ultrastructural observations of Papaver rhoeas mature pollen grains. Bot. Acta 103: 349–354.
Dietrich, A., Mayer, J.E. and Hahlbrock, K. (1990) Fungal elicitors trigger rapid, transient and specific protein phosphorylation in parsley cell suspension cultures. J. Biol. Chem. 265: 6360–6368.
Elleman, C.E., Franklin-Tong, V.E. and Dickinson, H.G. (1992) Pollination in species with dry stigmas. The nature of the early stigmatic response and the pathway taken by pollen tubes. New Phytol. 121: 413–424.
Foote, H.C.C., Ride, J.P., Franklin-Tong, V.E., Walker, E.A., Lawrence, M.J. and Franklin, F.C.H. (1994). Cloning and expression of a distinctive class of self-incompatibility (S) gene from Papaver rhoeas. Proc. Natl. Acad. Sci. U.S.A. (in press).
Franklin, F.C.H., Hackett, R.M. and Franklin-Tong, V.E. (1992) Molecular studies of the pollen-stigma interaction. In: J.A. Callow and J.G. Green (eds.), Perspectives in Plant Cell Recognition, pp. 79–103. SEB Seminar Series, Cambridge University Press, Cambridge.
Franklin, F.C.H., Franklin-Tong, V.E., Thorlby, G.J., Atwal, K.K. and Lawrence, M.J. (1991) Molecular basis of the self-incompatibility mechanism in Papaver rhoeas L. Plant Growth Regulation 11: 5–12.
Franklin-Tong, V.E. and Franklin, F.C.H. (1992) Gametophytic self-incompatibility in Papaver rhoeas L. Sex. Plant Reprod. 5: 1–7.
Franklin-Tong, V.E., Lawrence, M.J. and Franklin, F.C.H. (1988) An in vitro bioassay for the stigmatic product of the self-incompatibility gene in Papaver rhoeas L. New Phytol. 110: 109–118.
Franklin-Tong, V.E., Ruuth, E., Marmey, P., Lawrence, M.J. and Franklin, F.C.H. (1989) Characterization of a stigmatic component from Papaver rhoeas L. which exhibits the specific activity of a self-incompatibility (S-) gene product. New Phytol. 112: 307–315.
Franklin-Tong, V.E., Lawrence, M.J. and Franklin, F.C.H. (1990) Self-incompatibility in Papaver rhoeas L.: inhibition of incompatible pollen tube growth is dependent on pollen gene expression. New Phytol. 116: 319–324.
Franklin-Tong, V.E., Atwal, K.K., Howell, E.C., Lawrence, M.J. and Franklin, F.C.H. (1991) Self-incompatibility in Papaver rhoeas L.: there is no evidence for the involvement of stigmatic ribonuclease activity. Plant Cell and Environ. 14: 423–429.
Franklin-Tong, V.E., Lawrence, M.J., Thorlby, G.J. and Franklin, F.C.H. (1992) Recognition, signals and pollen responses in the incompatibility reaction in Papaver rhoeas. In: E. Ottaviano, D.L. Mulcahy and G. Mulcahy-Bergamini (eds.), Angiosperm Pollen and Ovules, pp. 84–93. Springer-Verlag, New York (in press).
Franklin-Tong, V.E., Ride, J.P., Read, N.D., Trewavas, A.J. and Franklin, F.C.H. (1993) The self-incompatibility response in Papaver rhoeas is mediated by cytosolic free calcium. The Plant J. 163–177.
Gray, J.E., McClure, B.A., Bonig, I., Anderson, M.A. and Clarke, A.E. (1991) Action of the style product of the self-incompatibility gene of Nicotiana alata (S-RNase) on in vitro-grown pollen tubes. The Plant Cell 3: 271–283.
Heslop-Harrison, J., Knox, R.B. and Heslop-Harrison, Y. (1974). Pollen wall proteins. Exine-held fractions associated with the incompatibility response in Crucifera. Theor. Appl. Genet. 44: 133137.
Heslop-Harrison, Y. and Shivanna, K.R. (1977) The receptive surface of the Angiosperm stigma. Ann. Bot. 41: 1233–1258.
berger, T.R., Golke, J.R., Xu, B. and Kao, T-H. (1991) Primary structural features of the self-incompatibility protein in the Solanaceae. Sex. Plant Reprod. 4: 81–87.
Jepson, I. (1989) An approach to cloning the self-incompatibility gene in Papaver rhoeas, the field poppy. Ph.D. thesis, University of Birmingham, Birmingham.
Lane, M.D. and Lawrence, M.J. (1993). The population genetics of the self-incompatibility polymorphism in Papaver rhoeas. VII. The number of S-alleles in the species. Heredity 71: 596–602.
Lawrence, M.J. (1975) The genetics of self-incompatibility in Papaver rhoeas L. Proc. R. Soc. London Ser. B. 188: 275–285.
Lawrence, M.J. and O’Donnell, S. (1981) The population genetics of the self-incompatibility polymorphism in Papaver rhoeas III. The number and frequency of S-alleles in two further natural populations. Heredity 47: 53–61.
Lawrence, M.J., Afzal, M. and Kenrick, J. (1978) The genetical control of self-incompatibility in Papaver rhoeas. Heredity 40: 239–253.
Lewis, D.H. (1980) Are there inter-relations between the metabolic role of boron, synthesis of phenolic phytoalexins and the germination of pollen? New Phytol. 84: 261–270.
Lundqvist, A. (1964) The genetics of incompatibility. In: Genetics Today, Proc. XI Int. Congr. Genetics, 1963, pp. 637–647.
Mascarenhas, J.P. (1966) Pollen tube growth and RNA synthesis by vegetative and generative nuclei of Tradescantia. Am. J. Bot. 53: 563–569.
Mascarenhas, J.P. (1975) The biochemistry of Angiosperm pollen development. Bot. Rev. 41: 259–314.
McClure, B.A., Haring, V., Ebert, P.R., Anderson, M.A., Simpson, R.J., Sakiyama, F and Clarke, A.E. (1989) Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342: 955–957.
McClure, B.A., Gray, J.E., Anderson, M.A. and Clarke, A.E. (1990) Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347: 757–760.
McNaughton, I.H. and Harper, J.L. (1960) The comparative biology of closely related species living in the same area. I. External breeding barriers between Papaver species. New Phytol. 59: 15–26.
Michell, R.H. (1975) Inositol phospholipids and cell surface receptor function. Biochim. Biophys. Acta 415: 81–147.
Miller, D.D., Callaham, D.A., Gross, D.J. and Hepler, P.K. (1992) Free CaZ* gradient in growing pollen tubes of Lilium. J. Cell Sci. 101: 7–12.
Nasrallah, J.B., Kao, T-H., Goldberg, M.L. and Nasrallah, M.E. (1985) A cDNA clone encoding an S-specific glycoprotein from Brassica oleracea. Nature 318: 263–267.
Newton, W.C.F. (1929) The inheritance of flower colour in Papaver rhoeas and related forms. J. Genet. 21: 398–404.
Obermeyer, G. and Weisenseel, M.H. (1991) Calcium channel blocker and calmodulin antagonists affect the gradient of free calcium ions in lily pollen tubes. Eur. J. Cell Biol. 56: 319–327.
Polya, G.M., Micucci, V., Rae, A.L., Harris, P.J. and Clarke, A.E. (1986) CaZ*-dependent protein phosphorylation in germinated pollen of Nicotiana alata, an ornamental tobacco. Physiol. Planta. 67: 151–157.
Rathore, K.S., Cork, R.J. and Robinson, K.R. (1991) A cytoplasmic gradient of CaZ* is correlated with the growth of lily pollen tubes. Dev. Biol. 148: 612–619.
Rogers, S. (1969) Studies on British poppies. I. Some observations on the reproductive biology of the British species of Papaver. Watsonia 7: 55–63.
Singh, A., Perdue, T.D. and Paolillo, D.J., Jr. (1989) Pollen-pistil interactions in Brassica oleracea: cell calcium in self and cross pollen grains. Protoplasma 151: 57–61.
Stein, J.C., Howlett, B., Boyes, D.C., Nasrallah, M.E. and Nasrallah, J.B. (1991) Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc. Natl. Acad. Sci. U.S.A. 88: 8816–8820.
Teasdale, J., Daniels, D., Davis, W.C., Eddy, R. and Hadwiger, L.A. (1974) Physiological and cytological similarities between disease resistance and cellular incompatibility responses. Plant Physiol. 54: 690–695.
Trewavas, A.J. and Gilroy, S. (1991) Signal transduction in plant cells. Trends Genet. 7: 356–361.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1994 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Franklin-Tong, V.E., Lawrence, M.J., Franklin, F.C.H. (1994). The molecular and cellular biology of gametophytic self-incompatibility in Papaver rhoeas . In: Williams, E.G., Clarke, A.E., Knox, R.B. (eds) Genetic control of self-incompatibility and reproductive development in flowering plants. Advances in Cellular and Molecular Biology of Plants, vol 2. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-1669-7_3
Download citation
DOI: https://doi.org/10.1007/978-94-017-1669-7_3
Publisher Name: Springer, Dordrecht
Print ISBN: 978-90-481-4340-5
Online ISBN: 978-94-017-1669-7
eBook Packages: Springer Book Archive